Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon, Tamaulipas, Mexico

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ZooKeys 417: 103-132 (2014)

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Diversity and altitudinal distribution of Chrysomelidae
(Coleoptera) in Peregrina Canyon, Tamaulipas, Mexico

Uriel Jeshua Sanchez-Reyes', Santiago Nifio-Maldonado?, Robert W. Jones?

| Division de Estudios de Posgrado e Investigacién. Instituto Tecnolégico de Cd. Victoria. Boulevard Emilio
Portes Gil No.1301, C.P 87010. Ciudad Victoria, Tamaulipas, México 2 Facultad de Ingenieria y Cien-
cias. Universidad Auténoma de Tamaulipas. Centro Universitario Victoria. CP 87149. Victoria, Tamaulipas,
México 3 Facultad de Ciencias Naturales. Universidad Auténoma de Querétaro. Avenida de las Ciencias, s/n,
76230 Juriquilla, Querétaro, México

Corresponding author: Santiago Nino-Maldonado (email address)

Academic editor: A. Konstantinov | Received 19 March 2014 | Accepted 27 May 2014 | Published 19 June 2014
Attp.//zoobank.org/D8630AC3-E8 1 B-4C9B-94A6-F69E1F596BFC

Citation: Sanchez-Reyes UJ, Nifio-Maldonado S, Jones RW (2014) Diversity and altitudinal distribution of Chrysomelidae
(Coleoptera) in Peregrina Canyon, Tamaulipas, Mexico. ZooKeys 417: 103-132. doi: 10.3897/zookeys.417.7551

Abstract

The Chrysomelidae (Coleoptera) is a highly speciose family that has been poorly studied at the region-
al level in Mexico. In the present study, we estimated species richness and diversity in oak-pine forest,
Tamaulipan thorny scrub and in tropical deciduous forests in Peregrina Canyon within the Altas Cumbres
Protected Area of the northeastern state of Tamaulipas, Mexico. Sampling of Chrysomelidae consisted of
five sweep net samples (200 net sweeps) within each of three sites during four sample periods: early dry
season, late dry season, early wet season, and late wet season. Species were identified and total numbers
per species were recorded for each sample. A total of 2,226 specimens were collected belonging to six
subfamilies, 81 genera and 157 species of Chrysomelidae from the study area. Galerucinae was the most
abundant subfamily with 1,828 specimens, representing 82.1% of total abundance in the study area.
Lower abundance was recorded in Cassidinae (8.5%), Eumolpinae (3.6%), Cryptocephalinae (2.2%),
Chrysomelinae (2.2%), and finally Criocerinae (1.3%). The highest species richness was also presented in
the subfamily Galerucinae with 49% of the total obtained species followed by Cassidinae (20%), Crypto-
cephalinae (9.7%), Eumolpinae (9.7%), Chrysomelinae (6.5%) and Criocerinae (5.2%). The most com-
mon species were Centralaphthona fulvipennis Jacoby (412 individuals), Centralaphthona diversa (Baly)
(248), Margaridisa sp.1 (219), Acallepitrix sp.1 (134), Longitarsus sp.1 (104), Heterispa vinula (Erichson)
(91), Epitrix sp.1 (84) and Chaetocnema sp.1 (72). Twenty-two species were doubletons (1.97% of total
abundance) and 52 were singletons (2.33%). The estimated overall density value obtained was 0.0037 in-
dividuals/m2. The greatest abundance and density of individuals were recorded at the lowest elevation site.

However, alpha diversity increased with increasing altitude. Similarity values were less than 50% among

Copyright U,. Sanchez-Reyes et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

104 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

the three sites indicating that each site had distinct species assemblages of Chrysomelidae. The highest
abundance was obtained during the late dry season, whereas diversity indices were highest during the early
wet season. The present work represents the first report of the altitudinal variation in richness, abundance,
and diversity of Chrysomelidae in Mexico. These results highlight the importance of conservation of this

heterogeneous habitat and establish baseline data for Chrysomelidae richness and diversity for the region.

Keywords

Chrysomelidae, leaf beetles, species richness, abundance, altitude, Northeast Mexico

Introduction

Chrysomelidae is one of the largest families within the order Coleoptera, with over
35,000 species described worldwide (Jolivet et al. 2009). In Mexico, about 2,174 spe-
cies are known (Orddfez-Reséndiz et al. 2014), although the actual number is prob-
ably considerably greater. The family is also an economically important group due to
their predominantly phytophagous feeding habits (Ding et al. 2007, Meissle et al.
2009). This feeding characteristic and their generally high abundance also make leaf
beetles an important component of food webs and a major component of tropical her-
bivore guilds (Farrell and Erwin 1988, Basset and Samuelson 1996) as well as being an
important food item for other organisms (Eben and Barbercheck 1996).

The great species richness of Chrysomelidae and their role as a phytophagous func-
tional group make the Chrysomelidae a potentially useful indicator group for: 1) bio-
diversity of a region (Farrell and Erwin 1988, Kalaichelvan and Verma 2005, Baselga
and Novoa 2007, Aslan and Ayvaz 2009), 2) environmental quality (Linzmeier et al.
2006), and 3) as a taxon for monitoring changes in natural areas (Staines and Staines
2001, Flowers and Hanson 2003). However, the use of this family as such has not been
adequately explored. In addition, the general lack of published studies of the species
richness and diversity of Chrysomelidae in Mexico (Burgos-Solorio and Anaya-Rosales
2004, Andrews and Gilbert 2005, Nifo et al. 2005, Furth 2006, Furth 2009), makes
it dificult to compare the particular ecological characteristics and biogeographical dis-
tribution patterns of this family with other taxa in the country.

Recent climatic and environmental changes create an ecological imbalance that
threatens biodiversity. It is vital that baseline data is available through faunistic inven-
tories along elevational gradients to record and predict how organisms alter distribu-
tions and adapt to environmental changes (Maveety et al. 2011). This is especially so
for Mexico where altitude is often associated with marked changes in the richness and
abundance of species (Peterson et al. 1993), producing rapidly changing distribution
patterns along altitudinal gradients (Hodkinson 2005).

The present study was conducted in the Cafion of the Peregrina within Altas Cum-
bres Protected Area (Vargas et al. 2001) within the northeastern state of Tamaulipas,
Mexico. This protected area is located in one of the 15 panbiogeographic nodes in the
country. These nodes have unique characteristics which make them centers of higher
species richness with high conservation priority (Morrone and Marquez 2008) making

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 105

the study area an excellent site for analysis of biodiversity and altitudinal distribution
of Chrysomelidae in northern Mexico.

The objectives of the present study were: 1) determine the species richness of
Chrysomelidae in Peregrina Canyon, Tamaulipas, Mexico; 2) conduct the first site-
specific evaluation of diversity for this taxon in northeast Mexico; and 3) analyze the
variation of species richness, abundance and diversity of the family along an altitudinal
gradient during different seasons within the study area.

Methods

Study area

The Peregrina Canyon (Canyon San Felipe or Liberty), is located in the northwest
portion of municipality of Victoria, Tamaulipas, along the San Felipe River (Figure 1).
The area is located in the Sierra Madre Oriental and is part of Altas Cumbres Protected
Area, considered a Special Zone subject to Ecological Conservation established by state
decree in 1997 (Vargas et al. 2001). The study area belongs to one of the 15 panbio-
geographic nodes present in the country due to the overlap of three biotic provinces:
Tamaulipas, Sierra Madre Oriental, and Mexican Gulf (Morrone and Marquez 2008).
The altitude within the study area ranges from 340 to 1600 m. ‘The climate of the
region is warm and subhumid with summer rains; the mean annual temperature is 18
to 24.3 °C and the mean total annual rainfall is 717.3 mm to 1058.8 mm (Almaguer-
Sierra 2005).

Site location

Three sites were established within which five quadrants of 2500 m* (50x50 m) were
delineated in representative vegetation at each site. Site 1 had the lowest elevation at
340 m and consisted of low tropical semideciduous forest (23°45.30'N; 99°18.39'W).
Site 2 was located at an intermediate altitude at 550 m where the plant communi-
ty consisted of Tamaulipan thorny scrub (23°46.32'N; 99°14.96'W). Site 3 was the
highest site at 1100 m with the vegetation composed of oak-pine forest (23°46.62'N;
99°12.55'W).

Collection and processing of specimens

Sampling was conducted using a standard entomological sweep net of 40 cm diam-
eter. Individual samples consisted of 200 sweeps of the shrub and herbaceous vegeta-
tion in each quadrant. ‘The contents of the net were emptied into a 2000 cm’ plastic

bag, adding 60% ethanol and an indelible label with corresponding data. Samples

106 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

S
cy Location of
Peregrina Canyon

@ Victoria City

110°

101° ~—:100°

Altitudinal range (m)
190 - 380
/\/ 381 - 580
/\ / 581 - 740
741 - 900
901 - 1060
1061 - 1240
1241 - 1420
: as _/ 1421 - 1600
101° 100° . /\/ 1601 - 1820

99°36" 99°28! 99°20' 99°12" 98°56!
99°18! 99°42!

N

Sites of study within Peregrina Canyon
e@ Site 3 - Oak pine forest - 1100 m
@ Site 2 - Tamaulipan thorny scrub - 550 m
© Site 1 - Low tropical semideciduous forest - 340 m

)
Municipal limit
[__] Victoria City
Altitudinal range (m)
HM 220 - 336.25
MM 336.25 - 452.5
GM 452.5 - 568.75

() 568.75 - 685
[J 685 - 801.25

801.25 - 917.5

917.5 - 1033.75
[___] 1033.75 - 1150
[_] 1150 - 1266.25
[| 1266.25 - 1382.5
[my 1382.5 - 1498.75
[1498.75 - 1615
(iy 1615 - 1731.25
(1731.25 - 1847.5
[1847.5 - 1963.75

15 Kilometers 1963.75 - 2080

\ 3 Autor: Uriel Jeshua Sanchez Reyes
6 Source: INEGI, 2010. Datum WGS84,
me Geographical coordinates

99°18' 99°15" 99°12"

Figure |. Location of Peregrina Canyon in Tamaulipas, Mexico, and location of sampling sites along

study area.

were collected at each site from 10:00 to 14:00 hrs. Five samples (one sample for
each quadrant, 200 net sweeps) were taken within each of three sites (one site per
day), at four different dates in each of the four seasons of the year (early dry season,

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 107

EDR, December-February; late dry season, LDS, March-May; early wet season, EWS,
June-August; and late wet season, LWS, September-November) between January and
December 2009, for a total of 240 samples.

Processing of the samples was performed in the laboratory in the following man-
ner. First, the contents of each plastic bag (sample) were placed in a plastic tray with
water, and the more voluminous plant remains (wood fragments, branches, stems,
leaves) were removed. A sieve ALSA (0.175 mm) was then used to filter the sample,
and the reduced contents placed in a petri dish and observed under a stereoscopic mi-
croscope for extraction of all chrysomelid beetles. These were separated and mounted
on paper points according to standard entomological technique. All specimens are
stored in the collection of the Facultad de Ingenieria y Ciencias at the Universidad
Autoénoma de Tamaulipas, Ciudad Victoria, Tamaulipas, Mexico.

Taxonomic determination

The identification of the specimens was performed using the available literature on
Chrysomelidae (Wilcox 1965, White 1968, Wilcox 1972, Scherer 1983, White 1993,
Flowers 1996, Riley et al. 2002, Staines 2002). Where possible, the material was com-
pared with identified specimens deposited in the collection of Chrysomelidae of the
Facultad de Ingenieria y Ciencias, Universidad Autonoma de Tamaulipas. Those speci-
mens that could not be identified to the species level were compared with other uni-
dentified specimens and grouped into morphospecies. The designation of “species” in
this study includes both morphospecies and determined species. The classification used
in this work corresponds to latest taxonomic categories proposed by Riley et al. (2003),
except for the subfamily Bruchinae not included in this study.

Data analysis

Abundance was calculated using the number of individuals per species collected at
each site, season and for the entire study area. Species abundance was divided into five
categories: 1) very common (more than 70 individuals); 2) common (11 to 70); 3) rare
(10 to three specimens); 4) doubletons (two specimens); and 5) singletons (one speci-
men only). As a measure of species richness, we used the number of species present
throughout the Peregrina Canyon, in each of the three altitudinal strata analyzed, and
in each season. To estimate the potential number of species (total, site, and season),
the nonparametric estimators Chao 1 and Jackknife 1 were used. These estimators
were chosen because: 1) we did not assume a previous abundance distribution model,
2) they are robust when calculating minimum estimate of species richness, 3) their
use is recommended as a recurrent measure in analysis of biodiversity, 4) Chao 1 is
based on abundance data, or singletons and doubletons, and Jackknife 1 (incidence)
is based on uniques, or species found in only one sample (Magurran 2004, Hortal et

108 Uriel Jeshua Sdnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

al. 2006, Gotelli and Colwell 2010), and 5) Jackknife indices tend to be conservative
estimators, so the use of both Chao 1 and Jackknife 1 can give an estimated range of
species richness (Silva and Coddington 1996). The estimators were calculated with 100
randomizations without replacement using the software EstimateS 8.2 (Colwell 2009)
based on the number and abundance of species found per sampling unit (quadrant).
Sampling efficiency was also measured by using Clench model, through the coefh-
cient of determination (R’) and the slope of the species accumulation curve, which
measures the inventory quality. Their calculation was based on the number of samples
(quadrants) in the entire study area, site and season; the procedure was performed in
the program STATISTICA 8.0 (StatSoft Inc. 2007) based on the method described by
Jiménez-Valverde and Hortal (2003). We also calculated overall density, or number of
chrysomelid beetles per square meter for future comparisons and was calculated for the
entire study area and for each site and season.

After testing for normality of the data, we used the nonparametric Kruskall Wallis
and Mann-Whitney tests to analyze the differences in abundance and number of spe-
cies among the three sites and between different seasons (PAST version 1.94b, Ham-
mer et al. 2001) using as independent variables the total number of specimens and
species per sample unit (quadrant).

Alpha diversity for the whole study area and by site and season was calculated using
the Simpson diversity index (1/D) and the Shannon diversity index (H °) (Magurran
2004), using EstimateS 8.2. Differences of diversity values between sites and seasons were
analyzed using PAST version 1.94b (Hammer et al. 2001). SHE analysis of diversity was
conducted to decompose the Shannon diversity value in a measure of species richness and
evenness, to allow the interpretation of changes in diversity (Magurran 2004). As a beta
diversity measure, Bray-Curtis similarity index (Sorensen’s quantitative index; Magurran
2004) was used among the sites and seasons, using EstimateS 8.2; these data were used
to build a distance matrix for an agglomerative cluster analysis, using the Ward’s method
as amalgamation algorithm calculated using STATISTICA 8.0. A Spearman correlation
test was applied between precipitation and temperature data with ecological parameters
(abundance and species richness) using STATISTICA 8.0. Precipitation and temperature
data were obtained from a local meteorological station localized in Peregrina Canyon.

Results

Abundance, richness and diversity of Chrysomelidae in Peregrina Canyon

A total of 2,226 specimens of Chrysomelidae were collected from 240 samples from
May 2009 to April 2010, belonging to six subfamilies, 81 genera and 157 species
(Table 1). Galerucinae was the most abundant subfamily with 1,828 specimens, rep-
resenting 82.1% of total abundance in the study area. Lower abundance was recorded
in Cassidinae (8.5%), Eumolpinae (3.6%), Cryptocephalinae (2.2%), Chrysomelinae
(2.2%), and finally Criocerinae (1.3%). The highest species richness was also presented

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 109

Table |. Taxonomic list and abundance of Chrysomelidae by season and site in Peregrina Canyon,
Tamaulipas, Mexico. N = Total abundance; 1 = Low tropical semideciduous forest, 340 m; 2 = Tamauli-
pan thorny scrub, 550 m; 3 = Oak-pine forest, 1100 m.

Dry Season Wet Season

Early Late Early Late
(Dec - Feb) | (Mar - May) | (Jun - Aug) az “

Be | 253 | | 35 a3 [a [2

CASSIDINAE Gyllenhal, 1813
Tribu Chalepini Weise, 1910
Anisostena pilatei (Baly, 1864)
Brachycoryna pumila Guérin-Meéneville, 1844 LP c3
Chalepus bellulus (Chapuis, 1877)
Chalepus digressus Baly, 1885

Euprionota aterrima Guérin-Meéneville, 1844

Glyphuroplata sp. 1

Heterispa vinula (Erichson, 1847) IY 6

Octotoma championi Baly, 1885 2 2
Octotoma intermedia Staines, 1989 nit nahin 1
Sumitrosis inaequalis (Weber, 1801) jt 5
Sumitrosis pallescens (Baly, 1885) (he a esa eet al lle 1
Sumitrosis rosea (Weber, 1801) en Tae 8
Summitrosis sp. | (ean Da a Sa IE:
Summitrosis sp. 2 [ee a a a eS a eas
Xenochalepus (Neochalepus) chapuisi (Baly, 1885) ea et a) a ee | Lo 1
Xenochalepus (Xenochalepus) omogerus (Crotch,

1873) le z
Tribu Cassidini Gyllenhal, 1813

Charidotella bifossulata (Boheman, 1855) 1 3 | 1 5
Charidotella (Chaerocassis) emarginata 1 1
(Boheman, 1855)

Charidotella sexpunctata (Fabricius, 1781) i | aa Ta fa =F || |] 4
Charidotella tuberculata (Fabricius, 1775) ha | ge aes en | el | 2
Charidotis auroguttata Boheman, 1855 fey wee 1 Fel pea eee fi ae | 1
Tribu Cassidini Gyllenhal, 1813 ee ae a ee ey a el
Charidotella tuberculata (Fabricius, 1775) Se Pea Pia ey 2
Charidotis auroguttata Boheman, 1855 le eee See 1
Coptocycla (Psalidonota) texana (Schaeffer, 1933) a aS ee e)
Microctenochira punicea (Boheman, 1855) (Sahl a eal aS iad ee pe eee 5
Microctenochira varicornis (Spaeth, 1926) 1 1
Microctenochira vivida (Boheman, 1855) 1 1 2
Helocassis crucipennis (Boheman, 1855) 9 Be || 1 14
Helocassis testudinaria (Boheman, 1855) 1 tied Mz 5
Tribu Mesomphaliini Hope, 1840

Chelymorpha pubescens Boheman, 1854 1 1
Hilarocassis exclamationis (Linnaeus, 1767) i 1
Ogdoecosta juvenca (Boheman, 1854) 3» LAs 2 6
Tribu Ischyrosonychini Chapuis, 1875

Physonota alutacea Boheman, 1854 1 1

110

CHRYSOMELINAE Latreille, 1802
Tribu Chrysomelini Latreille, 1802
Subtribu Doryphorina Motschulsky, 1860

Dry Season

Early

(Dec - Feb)

1

3

—_

Late

Early
(Mar - May) | (Jun - Aug)

Uriel Jeshua Sanchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

Wet Season
Late

(Sep - Nov)

3
ame a a |
oma Pt | ||

Calligrapha fulvipes Stal, 1859
Calligrapha sp. 1

Calligrapha sp. 2
Calligrapha suffriani Jacoby, 1882

Labidomera suturella Chevrolat, 1844
Zygogramma piceicollis (Stal, 1859)

—

met NU] | DO fmt] me

Subtribu Chrysomelina Latreille, 1802
Chrysomela texana (Schaeffer, 1919)

Phaedon cyanescens Stal, 1860
Plagiodera semivittata Stal, 1860

Plagiodera thymaloides Stal, 1860
CRIOCERINAE Latreille, 1807

mS |

Tribu Lemini Heinze, 1962
Lema balteata LeConte, 1884

Lema sp. 1
Neolema quadriguttata White, 1993
Neolema sp. 1

—

Neolema sp. 2
Neolema sp. 3

Oulema sp. 1
Oulema sp. 2

Go | ee

CRYPTOCEPHALINAE Gyllenhal, 1813
Tribu Cryptocephalini Gyllenhal, 1813

Subtribu Cryptocephalina Gyllenhal, 1813
Cryptocephalus duryi Schaeffer, 1906

N

Cryptocephatus sp. 1
Cryptocephalus umbonatus Schaeffer, 1906

—_

Diachus auratus (Fabricius, 1801)
Subtribu Pachybrachina Chapuis, 1874

Pachybrachis sp. 1
Pachybrachis sp. 2
Pachybrachis sp. 3
Pachybrachis sp. 4
Pachybrachis sp. 5

—

Pachybrachis sp. 6
Pachybrachis sp. 7

—

NR MOPAR Nd {sy

Tribu Clytrini Lacordaire, 1848
Subtribu Clytrina Lacordaire, 1848

Anomoea rufifrons Chevrolat, 1837
Subtribu Megalostomina Chapuis, 1874

Coscinoptera scapularis scapularis (Lacordaire,
1848)

Nn
a) N Qo N N

— aa: me | Re W]e

rm | Oo
— — — iW) — — — Oo |e oe Meee’
yd N N — Oo
bo — — — WO }1N
So] | iA [hl SC i | a] [PSS] ill

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 111
Dry Season Wet Season
Early Late Early Late N
(Dec - Feb) | (Mar - May) | (Jun - Aug) | (Sep - Nov)
1 2taiifatstilats tite 3

Coscinoptera victoriana L.. Medvedev, 2012 1
Subtribu Babiina Chapuis, 1874
Babia tetraspilota LeConte, 1858 2 2
Tribu Chlamisini Gressitt, 1946
Chlamisus texanus (Schaeffer, 1906) 3 3
Neochlamisus sp. 1 1 1
EUMOLPINAE Hope, 1840
Tribu Eumolpini Hope, 1840
Brachypnoea sp. | (eae a ae E
Brachypnoea sp. 2 (em ad We
Chalcophana cincta Harold, 1874 De a a a ae 4|5
Colaspis melancholica Jacoby, 1881 [aa pee fm Pl a= Sra 1
Colaspis sp. | i Ope TT pe a
Colaspis townsendi Bowditch, 1921 = ie Te ie ae SES ci &
Tymnes sp. 1 i Ee ee:
Zenocolaspis inconstans Bechyné, 1997 (a ee See 3
Taga dentally 1663 fa ieee fat
Fidia albovittata Lefevre, 1877 [em 0 he] hl ed ES | i ea 1
Xanthonia sp. 1 Lo all pel 3 1 11
Xanthonia sp. 2 3 3
Xanthonia sp. 3 1 | 4 5
Xanthonia sp. 4 1 ii 8
Xanthonia sp. 5 1] 1 2
Tribu Typophorini Chapuis, 1874
Typophorus nigritus (Fabricius, 1801) 1 1
GALERUCINAE Latreille, 1802
Tribu Alticini Newman, 1835
Acallepitrix sp. 1 Z S| Oe Sle. be ill 29/3 1 | 134
Acallepitris: sp. 2 fo SE eS
Acallepitri: sp. 3 34] 5 St ae] aes [Pe 5 | [Las ias
Acallepitris: sp. 4 | as Mn 5 js fe] 8 om a
Acallepitrix sp. 5 a Ga a aT | a
Acrocyum dorsalis Jacoby, 1885 ae ait sil ee a |e 1
Alagoasa bipunctata (Chevrolat, 1834) fee] pee ceed MP ja a Fae hh neh | a 3
Alagoasa decemguttatus (Fabricius, 1801) ee eS eae 1 | 10
Alagoasa sp. 1 nnn ee Be
Asphaera abdominalis (Chevrolat, 1834) Se ee ee See 2 |. 12
Asphaera sp. | Fa FS a
Asphaera sp. 2 1 1
Asphaera sp. 3 1 1
Asphaera sp. 4 1 1
Blepharida rhois (Forster, 1771) 1 1
Centralaphthona diversa (Baly, 1877) 6: |(80. 66.) #P | 522) 30 14 33 | 25] 1 |248
Centralaphthona fulvipennis (Jacoby, 1885) 309} 1 42 3 56 1 |412

112 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

Dry Season Wet Season
Early Late Late N
(Dec - Feb) ar May) | (Jun - Aug) ae a“
Ho) || 539] fa| 34 1}2 2h stitatsiita2)

Chaetocnema sp. 1 27 \h2 9 ee
Chaetocnema sp. 2 1 8
Chaetocnema sp. 3 al Le 1 3 25
Derocrepis sp. 1 5
Derocrepis sp. 2 Zz
Disonycha antennata Jacoby, 1884 1 1
Disonycha glabrata (Fabricius, 1781) 1 8
Tribu Alticini cont
Disonycha stenosticha Schaeffer, 1931 | a a 2
Epitric sp. | 20 Fuca 3 | 84
Epitrix fasciata Blatchley, 1918 2 | ep | Ah | oe
Epitric sp. 3 Seine es aE
Glenidion sp.1 hE eta i
Heikertingerella sp. \ SS=— te [viele Fg | 2
Heikertingerella sp. 2 Rath 1) nl a
Heikertingerella variabilis (Jacoby, 1885) = See Pn ee 7
Longitarsus sp. 1 8 ea i ei 104
Longitarsus sp. 2 Camera nl 1
Longitarsus sp. 3 1 it V4
Longitarsus sp. 4 1
Longitarsus sp. 5 Tal 2 21
Lupraea sp. 1 13 18 | 32
Lupraea sp. 2 8 8
Lupraea sp. 3 16} 1 | 7 | 24
Lupraea sp. 4 26} 6 | 1 | 33
Lysathia sp. 1 1
Margaridisa sp. \ Sve 29 295) 219
Margaridisa sp. 2 1 1 3 | 6
Monomacra sp. 1 é Pa ee 4 | 33
Monomacra sp. 2 a ae era a ee 6
Monomacra sp. 3 Sr rhs Wall ast | Dos 1
Omophoita cyanipennis octomaculata (Crotch,
0 oe eben || eter
Orthaltica sp. 1 + |} ts) ai: al 5
Orthaltica sp. 2 1
Parchicola sp. 1 2 1 3
Phyllotreta sp. | 3 | 1 8
Plectrotetra sp. 1 18
Scelidopsis rufofemorata Jacoby, 1888 1
Tribu Alticini cont
Sphaeronychus fulvus (Baly, 1879) 1 5
Strabala sp. | 1
Syphrea sp. 1 2 1 22
Syphrea sp. 2 lila? 13

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 113

Dry Season Wet Season
Early Late Early Late
(Dec - Feb) | (Mar - May) | (Jun - Aug) | (Sep - Nov)
1 3 3
if

1 Eo

—_

Systena contigua Jacoby, 1884 27

Systena sp. 1

Walterianella signata (Jacoby, 1886)
Tribu Galerucini Latreille, 1802
Grupo Coelomerites Chapuis, 1875

Coraia subcyanescens (Schaeffer, 1906)

Derospidea cyaneomaculata (Jacoby, 1886)
Trirhabda sp. |

Grupo Schematizites Chapuis, 1875
Ophraea rugosa Jacoby, 1886

Tribu Luperini Chapuis, 1875
Subtribu Diabroticina Chapuis, 1875
Grupo Diabroticites Chapuis, 1875

Acalymma vittatum (Fabricius, 1775)
Diabrotica balteata LeConte, 1865
Diabrotica porracea Harold, 1875
Diabrotica underwoodi Bowditch, 1911
Gynandrobrotica lepida (Say, 1835)

Grupo Cerotomites Chapuis, 1875

Cerotoma atrofasciata Jacoby, 1879 1
Cerotoma ruficornis (Olivier, 1791) 1
Cyclotrypema furcata (Olivier, 1808)

Neobrotica sexmaculata Jacoby, 1887

Neobrotica tampicensis Blake, 1966

Subtribu Luperina Chapuis, 1875

WS)
—
— i
No
—
bee ae al
pet | et | Qo | —

Nn

—
—
Oo
\o
Nn

5

RS fm |N | |

Grupo Monoleptites Chapuis, 1875

es TY Ee ES] ls foal aL
—
iN
Se

Calomicrus sp. 1 1

in the subfamily Galerucinae with 49% of the total obtained species followed by Cas-
sidinae (20%), Cryptocephalinae (9.7%), Eumolpinae (9.7%), Chrysomelinae (6.5%)
and Criocerinae (5.2%).

Eight species were categorized as “very common” in the Peregrina Canyon, each
with greater than 70 specimens and accounted for 61.22% of the total abundance.
These very common species were Centralaphthona fulvipennis Jacoby (412 individuals),
Centralaphthona diversa (Baly) (248), Margaridisa sp.1 (219), Acallepitrix sp.1 (134),
Longitarsus sp.1 (104), Heterispa vinula (Erichson) (91), Epitrix sp.1 (84) and Chaetoc-
nema sp.1 (72). Twenty-five species were considered common, constituting 22.66% of
the total number of chrysomelids. Fifty species were considered rare (263 specimens)
by occupying 11.8% of the total abundance. Twenty-two species were doubletons
(1.97% of total abundance) and 52 were singletons (2.33%). The estimated density
value obtained was 0.0037 individuals/m? (Table 2).

114 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

Table 2. Richness, abundance and diversity parameters of Chrysomelidae in the Peregrina Canyon,
Tamaulipas, Mexico. S obs = Observed richness; N = Abundance; Dst = Density; S est = Estimated

richness; R* = Clench model determination coefficient; 1/D = Simpson diversity index; H’= Shannon

diversity index.

Site

aud me ne aa Tamaulipan | Oak-pine nies Total
arameter | semideciduous éhosiy sob Late
forest (Dec-Feb) | (Mar-May)
85a Gab
S est
Chao 1 84.41 | 218.45
Jackknife 1 126.48 150.31 1235 55.78 1973 130,22) 84.52 | 216.75
Clench
R 0.997 0.998 0.999 0.998 0.998 0.999 0.999 0.997
S est 128.49 171.80 133.91 57.70 143.46 E7559 94.85 212.41
Slope 0.368 0.532 0.395 0.187 0.539 0.729 0.385 0.178
Diversity *
1/D 5.93a: 10.12b 19.26c 4.28d 17.31a 24.66b 13.92c 14.6
ai 2.73a 3.24b 3.67c 2.17d 3,49a 3.78b 3.06c 3.54

Values with different letters within rows are significantly different using Kruskal-Wallis and Mann-Whit-
ney Tests: abundance between sites, K=15.92, DF=2, p=0.0003; richness between sites, K=8.17, DF=2,
p=0.0157; abundance between seasons, K=42.42, DF=3, p=0.000; richness between seasons, K=50.15,
DF=3, p=0.000.

* Diversity values with different letters within rows are significantly different at p<0.05, using permutation

and bootstrap tests in PAST program.

The richness estimators indicated that the total number of chrysomelid species in
the study area was between 216 and 218 species (Table 2, Figure 2) suggesting that the
observed total of 157 species represented 71.86 to 72.43% of the actual richness. The
data showed a good fit to the Clench model (R’ = 0.99), with a registered proportion
of species of 73.91% and a slope close to 0.1. Total diversity values of Chrysomelidae
in Peregrina Canyon were 14.58 for the Simpson index and 3.53 for the Shannon
index (Table 2). The SHE analysis shows that changes in Shannon diversity value are
attributed to increase and stability of species richness curve (Figure 3).

Altitudinal variation of Chrysomelidae

The abundance of chrysomelid beetles was significantly different among the three sites
(Table 2). The greatest abundance and density (individuals per square meter) were re-
corded at the lowest elevation site, and decreased with increasing altitude (Table 2). The
middle altitude site (Site 2) had the greatest number of species (Table 2). The number

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 115

Species richness

1 21 41 61 81 101 121 141 161 181 201 221 241

we 5 .5,010ek

Species richness

—- Sobs
-e- Chao 1
---- Jack 1

1 #5 9 13 17 21 25 29 33 37 41 #45 #49 #53 S57 61 65 69 73 77 81

Samples

Figure 2. Species accumulation curves by altitudinal site in the Peregrina Canyon, Tamaulipas, Mexico.
Upper graphic: accumulation curves for all study area. Lower graphic: site 1 (green color), site 2 (red

color) and site 3 (blue color).

of species significantly differed only between the lowest and the highest altitudinal strata
(Site 1 and Site 3; Table 2). In the low altitude site, 85 species were recorded which rep-
resented between 67.2 to 71.35% of the estimated richness (minimum and maximum)

116 Uriel Jeshua Sdanchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

| Total Peregrina Canyon 4.81 Site 1, Low tropical semideciduous forest
340 m

Diversity
Diversity

250 500 750 1000 1250 1500 1750 2000 120 240 360 480 600 720 840 960 1080
N N

Site 3, Oak pine forest, 1100 m

scrub, 550 m

Diversity

80 160 240 320 400 480 560 640 50 100 150 200 250 300 350 400 450
N N

Figure 3. SHE analysis of diversity for the Peregrina Canyon and for each one of altitudinal sites. In

S natural logarithm of species richness; In E natural logarithm of evenness; H diversity (Shannon index).

with the models used. In the second site, the number increased to 96 species (48.96
to 63.86% of the estimate) and at the highest site, 84 species were recorded (59.62 to
68.01% of the estimate) (Figure 2). A determination coefficient greater than 0.99 was
obtained for all sites, indicating a good fit of the Clench model to the data obtained at
each site, but the slope calculated was greater than 0.1 in all sites (Table 2).

Alpha diversity at the three sites differed significantly (p < 0.05) with indices increasing
progressively with increasing altitude (Table 2). Lower diversity values in both sites 1 and
2, were a result of a reduction in eveness and a more or less stable number of species with
the increase of samples. In site 3, diversity increases as eveness remained constant and the
number of species increased with sample numbers (Figure 3). Of the 157 species recorded
in the Peregrina Canyon, 34 were distributed along the entire altitudinal gradient, 40 were
recorded only in two sites, and 83 were unique to one of the three sites. Of these, 29 were
exclusively from Site 1, 34 for Site 2, and 20 for Site 3 (Table 1). Similarity values were
in all cases less than 50%; according to the cluster analysis, each of the three sites was an
independent group, containing distinct species assemblages of Chrysomelidae (Figure 4).

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 117

Low tropical
semideciduous
forest
(340 m)

Tamaulipan
thorny scrub
(550 m)

Oak-pine forest
(1100 m)

0.52 0.54 0.56 0.58 0.60 0.62 0.64

Linkage distance

Figure 4. Cluster analysis from sites in the Peregrina Canyon, Tamaulipas, Mexico.

Seasonal variation of Chrysomelidae

General abundance of Chrysomelidae was greater in the dry season than the wet sea-
son. Late wet season was not significantly different from early dry and wet seasons; the
rest of comparisons between seasons were significantly different. The highest abun-
dance was obtained during the late dry season, with 822 individuals. Fewer individu-
als were found during the early dry season (696 specimens), and late and early wet
seasons, 406 and 302, respectively. Density for seasons followed the same pattern as
the abundance, being late dry season the period with higher densities of chrysomelid
beetles (Table 2). The number of species collected per season declined as the year pro-
gresses. During late dry season, 96 species were recorded, representing between 69.91
and 72.72% of the estimated richness for that season; 84 species were found in early
wet season (62.36 to 64.5% of estimated richness), while the number decreases to 56
species in late wet season (66.25 to 66.34%) and 43 species in early dry season (77.08
to 87.66%) (Table 2; Figure 5). Determination coefficients based on the Clench model
was higher than 0.99 for all seasons, while the slope values were above 0.1 (Table 2).
Higher temperatures and precipitation were found within both wet seasons (Figure 6).
High correlation values were present between temperature and richness, and between
precipitation and abundance. Abundance was negatively correlated with precipitation,
while species richness was positively correlated with maximum temperature. Other
comparisons were not significant (Table 3).

In contrast to abundance, the Shannon and Simpson indices indicated the highest
diversity during the early wet season. Lower values of diversity occurred in late dry sea-

118 Uriel Jeshua Sanchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

140 —_—___—_—

WET SEASON

120

100

tars
eooree oo-gee lo Oe esti

ae goa

80

ate, e

ee eh OO
Pr etal es ciate Bo
er aon On

60

Species richness

40

20
—- Sobs

-e- Chao 1
-+- Jack 1

1 #4 7 10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55 58 61

DRY SEASON
140

120

100

80

60

ahh

me dndee id ot Adee & and

Cc eteeetnowrs ses © 0 00-00 6 © o 0-06-60 6 0-68
soa”

Ane

Species richness

40

20

--- Jack 1

1 4 7 10 13 16 19 22 25 28 31 34 37 40 43 46 49 52 55 58 61

Samples

Figure 5. Species accumulation curves by season in the Peregrina Canyon, Tamaulipas, Mexico. Upper
graphic: Early wet season (blue color) and late wet season (red color). Lower graphic: Early dry season

(black color) and late dry season (green color).

son, followed by late wet and early dry seasons. Based on diversity indices, all seasons
were statistically different (p < 0.05) (Table 2). Reduction in diversity value at early dry
season was originated by the drop in evenness with the increase of samples. ‘The rest of

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 119

Table 3. Spearman rank order correlations of abundance and species richness of Chrysomelidae with

precipitation and temperature in Peregrina Canyon; marked (*) correlations are significant at p < 0.05.

Richness
Precipitation 0.112
Max °C 0.842*
Min °C 0.587
Cy
<q
= 40 250
3
oO
<
§ 35
= 200
=
= 30 e
Ga Ss
e, 4 25
om 150 :
25 ;
Sop 20 S
g.2 E
Ean 100 =
@ 2 15 5
é 3
& A
= 10
& 50
g 5
=)
&
x
x 0 0
=
100 900
90 800
80 700 2
w
a" 600 §
2 60 &
2 500 €
& 50 na
ie 400 §
~ 40 §
a 300 &
2 30 5
2 2
20 200
10 100
0 0
EDS LDS EWS LWS
Early Dry Season Late Dry Season Early Wet Season Late Wet Season

Figure 6. Variation of Chrysomelidae with precipitation and temperature during 2009 in Peregrina

Canyon.

year, evenness values, remained constant with the increase of samples in each season
(Figure 7). Of the total species recorded in the annual period, only 13 were present
throughout the year, and 23 were registered in three seasons, 37 in only two, and 84
were unique to a single season. From these exclusive species, 38 were recorded in late
dry season, 26 in early wet season, 12 in late wet season, and only eight in early dry
season (Table 1). Bray Curtis index established the greatest similarity between early

120 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

Ee Early Dry Season

80 160 240 320 400 480 560 640 80 160 240 320 400 480 560 640 720
N N

Early Wet Season

30 60 90 120 150 180 210 240 270 50 100 150 200 250 300 350 400
N N

Figure 7. SHE analysis of diversity for each season in the Peregrina Canyon. In S natural logarithm of

species richness; In E natural logarithm of evenness; H diversity (Shannon index).

and late dry seasons (45.1%), and in descending order were presented late wet and
early dry seasons (38.8%), late dry and late wet seasons (37.9%), late dry and early wet
seasons (36.3%), early and late wet seasons (35.6%) and early wet and early dry seasons
(25.7%). The cluster analysis showed the formation of three groups according to the
composition of species in each season: the first group consists of the species present in
early and late dry seasons, the second group corresponds to late wet season species, and
the last group was the early wet season species (Figure 8).

Discussion
Species richness in Peregrina Canyon
There are few studies of the richness and diversity of Chrysomelidae in Mexico with

which the present study can be compared. Deloya and Ordéfiez (2008) reported 136
species in fragments of cloud forest, in the state of Veracruz, while Nifo et al. (2005)

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 121

Late dry season

a — I

Late wet season

Early wet season

0.4 0.5 0.6 0.7 0.8 0.9

Linkage distance

Figure 8. Cluster analysis from seasons in the Peregrina Canyon, Tamaulipas, Mexico.

presented a checklist of 128 species for Biosphere Reserve El Cielo in the state of
Tamaulipas, which also included cloud forest vegetation as well as tropical deciduous
habitats. Considering that both authors used similar methods to that applied in this
research, the 157 species found in this study is noteworthy for its greater richness.
This may be a result of the three distinct habitats sampled despite the greater aridness
of two of these (thorn scrub and oak forest) when compared to the habitats sampled
by Deloya and Ordéfez (2008) and Nifo et al. (2005). There are still other studies in
Mexico where the species richness or diversity has been analyzed; however, temporal
and spatial scale were greater, principally in those studies that were checklists in com-
plete states (Andrews and Gilbert 2005) and natural areas of greater extension (Or-
doniez-Reséndiz and Lépez-Pérez 2009, Orddfiez-Reséndiz et al. 2011), or also for all
the country and for only one subfamily or tribe, such Chrysomelinae (Burgos-Solorio
and Anaya-Rosales 2004), Alticini (Furth 2006, Furth 2009), Cassidinae (Martinez-
Sanchez et al. 2010) and Clytrini (Medvedev et al. 2012). Also these studies have been
made with very different methodologies and different approaches than in this study
which precludes a direct comparison with the results presented here.

Using the latest higher classification scheme of Riley et al. (2003), six subfamilies are
formally reported in this study (Table 1). Galerucinae had the greatest number of species
which is in accordance with subfamily species totals worldwide (Riley et al. 2002) and
in other studies with Chrysomelidae in different parts of the world, including Mexico
(Kalaichelvan and Verma 2005, Nino et al. 2005). The 157 species present in this work

122 Uriel Jeshua Sanchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

represent the 7.22% of the 2,174 reported species for México (Ordéfez-Reséndiz et al.
2014), which is a notable percentage considering the small area sampled in this study.
According to both non-parametrics estimators used, our data represent a sampling
efficiency superior to 70%. Similarly, Clench model indicated a percentage superior to
70% and a slope close to 0.1, indicating both data accuracy and the reliability of the
study (Jimenez-Valverde and Hortal 2003). However, richness estimators indicates that
the number of species is greater, thus a complementary method of sampling, such as
canopy fogging (Basset and Samuelson 1996, Novotny et al. 1999, Basset 2001, Charles
and Basset 2005, Vig and Marké 2005), malaise traps (Flowers and Hanson 2003), or
further sweep net samples (Sackmann 2006, Pedraza et al. 2010), would increase the
number of species found, as well as reducing the number of singletons and doubletons.
Alpha diversity of Chrysomelidae in Peregrina Canyon was high, and represents one
of the first known studies of site specific data for Mexico. Margalef (1972) notes that
Shannon index values are typically between 1.5 and 3.5, and rarely exceed a value of 4.
Based on this scale, it can be established that Chrysomelidae diversity in the study area
is high (Shannon = 3.53). These results can be explained in part by the geographic loca-
tion of the study area; Peregrina Canyon is located in one of the 15 panbiogeographic
nodes of Mexico, within the Sierra Madre Oriental. According to Morrone and Marquez
(2008), these areas are centers for high biological diversity, representing the confluence
of different biotic provinces. In this case, Peregrina Canyon is in the union of Tamauli-
pan, Sierra Madre Oriental and Mexican Gulf biotic provinces, thus presenting influ-
ences of both temperate and tropical faunas, which harbors high numbers of species in
the area and the typical pattern for tropical faunas, with a high percentage of singletons
and doubletons (Silva and Coddington 1996, Furth et al. 2003). This confluence of the
biotic provinces is evidenced by the biogeographic distribution of the collected species.
Considering the distribution for the identified species and the range of the genera for
morphospecies, a total of 71 species (both morphospecies and identified species) in this
study, (45%) were principally of Neotropical distribution (some ranging up to southern
states of USA, but with their major distribution through Mexico and south into Central
America and South America). This distribution is shared by many biotic groups of the
Mexican Gulf region (Morrone 2005). Another 24 species (15%) had typical Nearctic
distribution (Mexico north into the United States and Canada) which in Mexico in-
cludes the Tamaulipan province that extends north into Texas. Finally, 56 species (36%)
have distributions throughout the American continent (including North, Central and
South America), whereas 6 species (4%) were restricted to Mexico and possibly restricted
to or have originated within the Sierra Madre Oriental province. Further study of the
biogeographical distributions of the Chrysomelidae of Mexico is sorely needed.

Altitudinal and seasonal variation of Chrysomelidae

We present the first record of the altitudinal variation in richness, abundance, and diver-
sity of Chrysomelidae in Mexico. In our study, greater species richness was found in the

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 123

intermediate altitudes, which is a similar result to that found by Fernandez et al. (2010)
with Staphylinidae, where the number of species increased from first to second altitudi-
nal strata, and then decreased slightly in the highest part of the gradient. Greatest species
richness in intermediate altitudes has also been documented in Alticini (Chrysomelidae)
(Furth 2009), as well as dung beetles (Celi et al. 2004) and in some species of Scarabaei-
nae (Escobar et al. 2005). Intermediate areas represent an area of overlap in species dis-
tributions, which could explain the higher species richness in this site. Richness estima-
tors in each site indicated inventory completeness of less than 70%, with higher slopes
values for Clench model, which indicated a relatively incomplete inventory for each site
(Jimenez-Valverde and Hortal 2003). ‘This is due to the high number of doubletons and
singletons for each site which influenced the estimators used.

Decreasing abundance with increasing altitude has been observed in several studies
with other insects, such as necrophilic entomofauna (Sanchez-Ramos et al. 1993) and
ground beetles (Semida et al. 2001). In contrast to abundance, in this study there was
a progressive and significant increase in diversity with altitude, which was directly re-
lated to the altitudinal abundance recorded in each site. In the first site, the abundance
was very high, with some species concentrated in large numbers (e.g., C. fulvipennis),
thus reducing diversity. By contrast, in the higher elevation site, the Chrysomelidae
community is represented by a more equitative number of individuals, decreasing
dominance and thus increasing values of both diversity indices. This is confirmed by
the SHE analysis, where the evenness remain constant and the species richness increas-
es progressively with the increasing samples, being this pattern very different than the
other two sites. However, in a similar study with a different phytophagous group, Api-
onidae (Curculionoidea), Jones et al. (2012) found the opposite pattern with increas-
ing abundance with altitude but decreasing diversity, in the El Cielo Biosfera Reserve,
in Tamaulipas, Mexico. Also, Flowers and Hanson (2003) found that both species
richness and diversity of Alticini (Chrysomelidae) had lower values on higher altitudes
in Costa Rica. However, the pattern found in our study can be explained by the veg-
etation composition and the plant density in the sampled area, which was higher in
the semideciduous tropical forest site, with a greater number of herbaceous plants in
the understory. This characteristic is clearly an important factor for Chrysomelidae, be-
cause species are almost exclusively phytophagous, with species often highly specialized
and thus directly influenced by the composition of the vegetation and the presence and
abundance of their host plants (Ribeiro et al. 1994, Rehounek 2002, Aslan and Ayvaz
2009, Flinte et al. 2011, Linzmeier and Ribeiro-Costa 2013).

Novotny et al. (2006) present evidence that the single most important factor con-
tributing to high species diversity of insects in the tropics is the diversity of plants.
This would seem to be simplest explanation for the differences in richness, diversity
and abundance with altitude of leaf beetles in the present study. Although the abiotic
factors that change with altitude, such as precipitation, temperature, air currents, and
solar radiation (Lawton et al. 1987, Barry 2008) can certainly affect some aspects of
the biology of Chrysomelidae, the single most important factor in the abundance and
diversity of these beetles is clearly the presence of their host plants (Ribeiro et al. 1994,

124 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

Aslan and Ayvaz 2009, Sen and Gok 2009, Flinte et al. 2011). Each site in the present
study has markedly different plant communities with different species compositions,
densities and vegetation structure. This was reflected in equally different communities
and abundances of leaf beetles among the three sites, with less than 50% similarity in
species among sites. Adding to the vegetation differences were anthropogenic activities
(grazing, logging) observed around some of the quadrants where sampling was carried
out. Moderate disturbance can increase overall plant production and diversity (Con-
nell 1978, Huston 1979), and would have a similar effect on leaf beetles (Sen and
Gok 2009). Plants within disturbed vegetation patches are often colonizing species,
and so they represent young leaves and less chemical defenses (Wolda 1978, Jolivet
1988, Novotny and Basset 1998) which would favor high abundance of species within
some genera of Galerucinae, such as Centralaphtona Bechyné & Bechyné, Chaetoc-
nema Stephens, Epitrix Foudras and Longitarsus Berthold. ‘The increase in abundance
and species richness as a result of the disturbance of vegetation has been observed in
other studies with beetles (Dagobert et al. 2008, Sanchez-Reyes et al. 2012), including
Chrysomelidae (Linzmeier and Ribeiro-Costa 2009), because by altering the species
composition of a plant community, also alters species composition and abundance of
phytophagous beetles (Wasowska 2004).

On a temporal scale, the Chrysomelidae community followed a markedly seasonal
pattern, where the dry season was the most favorable for collection of this group in
the study area (greatest abundance and species richness). This is a pattern that was
also found in the subtropical region where the higher captures of insects occur in
the dry season. Linzmeier and Ribeiro-Costa (2008, 2013) found the major activities
of Chrysomelidae during spring/summer, before the rains. Nummelin and Borowiec
(1991) in Uganda, also found the peak densities of chrysomelid beetles (subfamily
Cassidinae) at the beginning of the dry season after the long rains. Jones et al. (2012)
found the greatest richness, diversity and abundance of Apionidae (Curculionoidea)
during the dry season in northeastern Mexico. In our study, the greatest number of
species and individuals were recorded during the late dry season, resulting in a constant
evenness with the increase of the samples; also, the diversity value significantly higher
obtained at the early wet season was originated by the high number of species and the
drop in abundance value, which can be reflected also in the SHE analysis, where even-
ness remains constant at the increase of the samples.

Results presented here can be partially explained by the indirect effect of precipita-
tion and temperature on the abundance and species richness, respectively. In this study,
abundance increases significantly as precipitation decreases, while species richness in-
creases significantly with an increasing in the maximum temperature. Influence of high
temperature present during the wet season has been observed in other studies with
Chrysomelidae in tropical areas (Linzmeier and Ribeiro-Costa 2008, 2013). There are
several reasons that are related to precipitation and temperature and which can explain
the seasonal differences. First, it is probable that many of the leaf beetles are in larval
stages during the wet season, and hence lesser abundance of adults was obtained dur-
ing that season, because we did not collect immatures. At the start of the rainy season,

Diversity and altitudinal distribution of Chrysomelidae (Coleoptera) in Peregrina Canyon... 125

plant density increases which represents greater food availability and new leaf tissues
are more palatable for developing immatures (Wolda 1978, Jolivet 1988, Novotny and
Basset 1998, Linzmeier and Ribeiro-Costa 2008, 2013). Second, with greater foliage
during the wet season, the foliar area in general increases dramatically which results in
populations being more “diluted” among the foliage. Thus, the chances of collecting
individuals per sweep is reduced because of the great area of foliage. And third, many
leaf beetles pass the dry season as adults in high concentrations in microhabitats unre-
lated to their host plant and vegetation type. There is evidence that beetles will fly away
from dry habitats to wetter ones during the dry season, especially to riparian vegetation
(Janzen 1973). However, the life-cycles of each species determines the pattern seen in
the Chrysomelidae community, and thus an analysis of each species, their host plant
and specific behavior needs to be taken in account (Linzmeier and Ribeiro-Costa 2013).

Although our data only considered a single canyon, beta diversity between sites at
different altitudes was high. Similarity values obtained for all comparisons of sites were
below 50%. Among the sites there was greater similarity of the first two altitudinal
sites, with the lower similarity at the higher site. This pattern apparently reflects the
greater difference between the tropical and temperate affinities of the vegetation and
associated chrysomelids between the lower sites (Neotropical affinities) with the higher
site (Nearctic affinities). Similarly, all comparisons between seasons had a similarity
less than 50%, and a high number of exclusive species to each season. ‘This pattern of
low similarity indicates a significant turnover of species with altitude, which could be
caused by the environmental heterogeneity of the area reflected in the different vegetal
communities along the altitudinal gradient, which is observed in the three groups
formed by the site cluster, and also the three groups (group 1: LWS and EDS; group
2: EWS; group 3: LDS) that were formed in seasonal cluster. However, we also found
high values of alpha diversity for each of the sites and analyzed seasons, which suggests
that biotic and abiotic factors present at each site and for each station generates unique
conditions for certain species of chrysomelid beetles.

Our results highlight the importance of conservation of a heterogeneous habi-
tat which can generate unique species compositions of highly diverse taxa, such as
Chrysomelidae. Results presented here establish baseline data for Chrysomelidae rich-
ness and diversity for the region and can serve as a reference study for future work
on the potential use of Chrysomelidae as indicator group of community diversity in
natural areas. However, further studies are still needed to analyze the importance of
environmental factors in the distribution and phenology of Chrysomelidae species and
possible changes to expect due to climate change.

Conclusions

A total of 2,226 specimens were collected belonging to six subfamilies, 81 genera and
157 species of Chrysomelidae from the study area. The greatest abundance and den-
sity of individuals were recorded at the lowest elevation site; however, alpha diversity

126 Uriel Jeshua Stnchez-Reyes et al. / ZooKeys 417: 103-132 (2014)

increased with increasing altitude, and species richness was higher at intermediate al-
titude. Similarity values were less than 50% among the three sites indicating that each
site had distinct species assemblages of Chrysomelidae.

The highest abundance and species richness was obtained during the late dry sea-
son, whereas diversity was higher during the early wet season. Geographical location of
the study area plus different vegetal compositions from the three sites sampled could
be the principal reason for the variation here found in Chrysomelidae communi-
ties with altitude and season. Also, precipitation and temperature may influence the
Chrysomelidae community in study area; however, both abiotic factors affect directly
the vegetal composition which is assumed to be the principal factor in determining leaf
beetle species composition and abundance.

The present work is one of the first specific area studies of Chrysomelidae con-
ducted in Mexico, in which both altitude and season are analyzed. The information
presented here provides baseline data that allow for comparisons of the diversity and
species richness of Chrysomelidae on a regional and national scale. This information
could be used as an initial step to analyze the potential use of Chrysomelidae as an
indicator group of biodiversity in Mexico.

Acknowledgments

The authors express their thanks to PROMEP for financial support to cover publish-
ing fees. We wish to thank to Itzcéatl Martinez Sanchez, Javier Alejandro Obregén
Zuniga, Niver Tarqui, Lucas Hernandez Hernandez, Ivette de Leén, Pablo Ochoa, y
Justo Sanchez for their help in fieldwork. Also, we thank the authorities responsible
of the Ecological Park Los Troncones, for their assistance given to the authors for the
realization of this study.

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